Chronic toxicity of five structurally diverse demethylase-inhibiting fungicides to the crustacean Daphnia magna: A comparative assessment

ENVIRONMENTAL TOXICOLOGY & CHEMISTRY, Issue 6 2009Enken Hassold
Abstract
Demethylase inhibitors (DMIs) are broad-spectrum fungicides that are ubiquitously used in agriculture and medicine.
They comprise chemically heterogeneous substances that share a common biochemical target in fungi, the inhibition of a specific step in sterol biosynthesis.
Several DMIs are suspected to disrupt endocrine-mediated processes in a range of organisms and to inhibit ecdysteroid biosynthesis in arthropods.
It is unclear, however, whether and, if so, to what extent different DMI fungicides have a similar mode of action in nontarget organisms, which in turn would lead to a common chronic toxicity profile.
Therefore, we selected a representative of each of the major DMI classes,-the piperazine triforine, the pyrimidine fenarimol, the pyridine pyrifenox, the imidazole prochloraz, and the triazole triadimefon,-and comparatively investigated their chronic toxicity to Daphnia magna.
No toxicity was detectable up to the limit of solubility of triforine (61 ,mol/L).
All other DMIs reduced reproductive success by delaying molting and development and by causing severe developmental abnormalities among offspring.
Prochloraz was most toxic (median effective concentration [EC50] for fecundity reduction, 0.76 ,mol/L), followed by fenarimol (EC50, 1.14 ,mol/L), pyrifenox (EC50, 3.15 ,mol/L), and triadimefon (EC50, 5.13 ,mol/L).
Mean effect concentrations for fecundity reduction were related to lipophilicity and followed baseline toxicity.
However, triadimefon and fenarimol (but none of the other tested DMIs) caused severe eye malformations among exposed offspring.
Affected neonates did survive, but a reduced ecological fitness can be assumed.
Offspring exposed to fenarimol in mater matured earlier.
The investigated different life-history parameters were affected in a substance-specific manner.
These qualitatively different toxicity profiles suggest additional, substance-specific mechanisms of action in D. magna that probably are related to an antiecdysteroid action.
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Assessment of the toxicity of mixtures of nickel or cadmium with 9,10-phenanthrenequinone to Daphnia magna: Impact of a reactive oxygen-mediated mechanism with different redox-active metals

ENVIRONMENTAL TOXICOLOGY & CHEMISTRY, Issue 7 2007Fangli Xie
Abstract
Recently, we showed that reactive oxygen species (ROS) formation was involved in the toxicity of the redox-active metal Cu and mixtures of Cu plus a photomodified polycyclic aromatic hydrocarbon (PAH), phenanthrenequinone (PHQ), to Daphnia magna.
It is unknown, however, if similar results can be observed for metals with lower or no redox activity and their mixtures with PHQ.
In the present study using D. magna, the toxicity of Ni, a weakly redox-active metal, and of Cd, a non-redox active metal, was examined with or without PHQ.
The abilities of Ni, Cd, PHQ, and binary mixtures of metal plus PHQ to generate ROS were measured using a 2,,7,-dichlorofluorescein fluorescence assay.
The results were compared with the results of Cu and mixtures of Cu plus PHQ from a recent study by our group.
The order of metal toxicity to D. magna was found to be Cd , Cu > Ni.
As with Cu/PHQ mixtures, synergistic toxicity was observed for mixtures of Ni and PHQ, whereas additive toxicity was observed for mixtures of Cd and PHQ.
Alone, PHQ had no impact on ROS levels in D. magna.
Nickel alone caused elevated ROS, which was further enhanced in the presence of PHQ.
Neither Cd nor Cd/PHQ mixtures increased ROS production.
Attenuation of toxicity and ROS production was observed in response to treatment with low concentrations of L -ascorbic acid.
These results indicate potential toxic interactions between metals and modified PAHs.
With redox-active metals, such as Cu and Ni, and modified PAHs, such as PHQ, these interactions can involve ROS formation.
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Development of a daphnia magna DNA microarray for evaluating the toxicity of environmental chemicals

ENVIRONMENTAL TOXICOLOGY & CHEMISTRY, Issue 4 2007Hajime Watanabe
Abstract
Toxic chemical contaminants have a variety of detrimental effects on various species, and the impact of pollutants on ecosystems has become an urgent issue.
However, the majority of studies regarding the effects of chemical contaminants have focused on vertebrates.
Among aquatic organisms, Daphnia magna has been used extensively to evaluate organism- and populationlevel responses of invertebrates to pollutants in acute toxicity or reproductive toxicity tests.
Although these types of tests can provide information concerning hazardous concentrations of chemicals, they provide no information about their mode of action.
Recent advances in molecular genetic techniques have provided tools to better understand the responses of aquatic organisms to pollutants.
In the present study, we adapted some of the techniques of molecular genetics to develop new tools, which form the basis for an ecotoxicogenomic assessment of D. magna.
Based on a Daphnia expressed sequence tag database, we developed an oligonucleotide-based DNA microarray with high reproducibility.
The DNA microarray was used to evaluate gene expression profiles of neonatal daphnids exposed to several different chemicals: Copper sulfate, hydrogen peroxide, pentachlorophenol, or ,-naphthoflavone.
Exposure to these chemicals resulted in characteristic patterns of gene expression that were chemical-specific, indicating that the Daphnia DNA microarray can be used for classification of toxic chemicals and for development of a mechanistic understanding of chemical toxicity on a common freshwater organism.
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Population growth of Daphnia magna under multiple stress conditions: Joint effects of temperature, food, and cadmium

ENVIRONMENTAL TOXICOLOGY & CHEMISTRY, Issue 5 2006Evelyn H. W. Heugens
Abstract
Aquatic organisms in the field often are exposed to combinations of stress factors of variousorigins.
Little is known of the interaction between different types of stressors; hence, the predictability of their joint effects is low.
Therefore, the present study analyzed the joint effects of temperature, food, and cadmium on the population growth rate of the water flea Daphnia magna.
The results revealed that temperature, food, and cadmium, as well as their interactions, were important factors that influenced life-history parameters and, as a consequence, the population growth rate of D. magna.
In general, population growth rate increased at high temperature and food level but decreased when cadmium was present.
The positive effect of temperature on population growth rate was smallest at limiting food levels.
Negative effects of cadmium on the growth rate were enhanced at elevated temperatures, whereas high food levels protected the daphnids from adverse effects of cadmium.
To avoid over- or underestimation regarding the toxicity of substances to field populations, results of standard toxicity tests should be applied in a location-specific way.
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Comparative toxicity of cadmium, zinc, and mixtures of cadmium and zinc to daphnids

ENVIRONMENTAL TOXICOLOGY & CHEMISTRY, Issue 1 2006Joseph R. Shaw
Abstract
Investigations were conducted to determine acute (48-h) effects of cadmium and zinc presented individually and in combination on Ceriodaphnia dubia, Daphnia magna, Daphnia ambigua, and Daphnia pulex.
Toxicity tests were conducted with single metals to determine lethal effects concentrations (lethal concentrations predicted for a given percent [x] of a population, LCx value).
These were used to derive metal combinations that spanned a range of effects and included mixtures of LC15, LC50, and LC85 values calculated for each metal and species.
In single-metal tests, 48-h LC50 values ranged from 0.09 to 0.9 ,mol/L and 4 to 12.54 ,mol/L for cadmium and zinc, respectively.
For each metal, D. magna was most tolerant and showed a different pattern of response from all others as determined by slope of concentration,response curves.
In the combined metal treatments, all daphnids showed a similar pattern of response when LC15 concentrations were combined.
This trend continued with few exceptions when LC15 concentrations of cadmium were combined with LC50 or LC85 values for zinc.
However, when this treatment was reversed (LC15, zinc + LC50 or LC85, cadmium), responses of all species except D. magna indicated less-than-additive effects.
For C. dubia, a near complete reduction in toxicity was observed when the LC15 for zinc was combined with LC85 for cadmium.
Multimetal tests with D. magna did not differ from additive.
Collectively, these studies suggest that D. magna may not be representative of other cladocerans.
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ENVIRONMENTAL TOXICOLOGY & CHEMISTRY, Issue 1 2005Randall J. Bernot
Abstract
Room-temperature ionic liquids (ILs) are considered to be green chemicals that may replace volatile organic solvents currently used by industry.
However, IL effects on aquatic organisms and ecosystems are currently unknown.
We studied the acute effects of imidazolium-based ILs on survival of the crustacean Daphnia magna and their chronic effects on number of first-brood neonates, total number of neonates, and average brood size.
Lethal concentrations of imidazolium ILs with various anions (X,) ranged from a median lethal concentration (LC50) of 8.03 to 19.91 mg L,1, whereas salts with a sodium cation (Na+ X,) were more than an order of magnitude higher (NaPF6 LC50, 9,344.81 mg L,1; NaBF4 LC50, 4765.75 mg L,1).
Thus, toxicity appeared to be related to the imidazolium cation and not to the various anions (e.g., CI,, Br,, PF,6, and BF,4).
The toxicity of imidazolium-based ILs is comparable to that of chemicals currently used in manufacturing and disinfection processes (e.g., ammonia and phenol), indicating that these green chemicals may be more harmful to aquatic organisms than current volatile organic solvents.
We conducted 21-d chronic bioassays of individual D. magna exposed to nonlethal IL concentrations at constant food-resource levels.
Daphnia magna produced significantly fewer total neonates, first-brood neonates, and average neonates when exposed to lower concentrations (0.3 mg L,1) of imidazolium-based ILs than in the presence of Na-based salts at higher concentrations (400 mg L,1).
Such reductions in the reproductive output of Daphnia populations could cascade through natural freshwater ecosystems.
The present study provides baseline information needed to assess the potential hazard that some ILs may pose should they be released into freshwater ecosystems.
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Development and field validation of a biotic ligand model predicting chronic copper toxicity to Daphnia magna

ENVIRONMENTAL TOXICOLOGY & CHEMISTRY, Issue 6 2004Karel A.C. De Schamphelaere
Abstract
In this study, we developed a toxicity model predicting the long-term effects of copper on the reproduction of the cladoceran Daphnia magna that is based on previously reported toxicity tests in 35 exposure media with different water chemistries.
First, it was demonstrated that the acute copper biotic ligand model (BLM) for D. magna could not serve as a reliable basis for predicting chronic copper toxicity.
Consequently, BLM constants for chronic exposures were derived by multiple regression analysis of 21-d median effective concentrations (EC50s; expressed as Cu2+ activity) versus physicochemistry from a large toxicity dataset and the results of an additional experiment in which the individual effect of sodium on copper toxicity was investigated.
The effect of sodium on chronic toxicity (log KNaBL = 2.91) seemed to be similar to its effect on acute toxicity (log KNaBL = 3.19).
However, in contrast to the acute BLM, no significant calcium, magnesium, or combined competition effect was observed, and an increase in proton competition and bioavailability of CuOH+ and CuCO3 complexes was noted.
Some indirect evidence was also found for some limited toxicity of complexes of copper with two of three tested types of dissolved organic matter.
Because the latter was only a minor effect, this factor was not included in the chronic Cu BLM.
The newly developed model performed well in predicting 21-d EC50s and no-observed-effect concentrations in natural water samples: 79% of the toxicity threshold values were predicted within a factor of two of the observed values.
It is clear, however, that more research is needed to provide information on the exact mechanisms that have resulted in different BLM constants for chronic exposures (as opposed to acute exposures).
It is suggested that the developed model can contribute to the improvement of risk assessment procedures of copper by incorporating bioavailability of copper in these regulatory exercises.
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ENVIRONMENTAL TOXICOLOGY & CHEMISTRY, Issue 1 2004Peter Carsten von der Ohe
Abstract
In the field, a multitude of species can be exposed to numerous toxicants; thus, the sensitivity of individual species to particular toxicants must be known to predict effects and to analyze changes in species composition.
For most species, no information about their toxicant sensitivity is available.
To address this limitation, we have grouped the available information to assign sensitivities to aquatic invertebrate taxa relative to Daphnia magna.
With respect to organic compounds, most taxa of the orders Anisoptera, Basommatophora, Coleoptera, Decapoda, Diptera, Ephemeroptera, Eulamellibranchiata, Heteroptera, Hirudinea, Isopoda, Oligochaeta, Prosobranchia, Trichoptera, Tricladida, and Zygoptera are less sensitive than D. magna.
Some taxa of the Amphipoda, Plecoptera, and Cladocera (other than D. magna) are significantly more sensitive.
For organic compounds, approximately 22% of the investigated taxa were more sensitive than D. magna.
Most taxa of the orders Amphipoda, Basommatophora, Diptera, Ephemeroptera, Eulamellibranchiata, Heteroptera, Isopoda, Oligochaeta, and Tricladida are significantly less sensitive than D. magna to metal compounds.
The taxa belonging to the Crustacea, with the exception of the order Isopoda, are much more sensitive.
For metal compounds, approximately 30% of the investigated taxa were more sensitive than D. magna.
Hence, D. magna is among the most sensitive taxa regarding both groups of toxicants.
The sensitivities for several taxa are listed, and use of the relative sensitivity distribution to link toxicant effects in mesocosm studies and field investigations is discussed.
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Postexposure feeding depression: A new toxicity endpoint for use in laboratory studies with Daphnia magna

ENVIRONMENTAL TOXICOLOGY & CHEMISTRY, Issue 6 2002Ruth A. McWilliam
Abstract
In situ bioassays with daphnids currently employ lethality as an endpoint, and although sublethal responses (reproduction and feeding rate) can be measured in the field, such endpoints pose major practical challenges.
Previous studies have indicated that Daphnia magna exposed to toxic substances can exhibit delayed recovery in feeding behavior (postexposure feeding depression).
This simple, robust response has the potential to be an ecologically relevant and potentially diagnostic endpoint.
This study developed and tested the use of postexposure feeding depression as a toxicity endpoint in the laboratory environment.
First, replicate numbers were manipulated to produce statistically reliable results.
Second, postexposure feeding depression in D. magna was studied under laboratory conditions, by employing toxic substances with differing modes of action.
Although most substances caused feeding inhibition during direct exposure, not all substances produced postexposure feeding depression.
However, the use of lethality as a supplementary endpoint provided an alternative measure when no feeding depression was apparent after exposure.
In combination, these endpoints offer a potentially more sensitive, ecologically relevant alternative to the use of lethality alone for in situ bioassay studies.
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Partitioning, bioavailability, and toxicity of the pyrethroid insecticide cypermethrin in sediments

ENVIRONMENTAL TOXICOLOGY & CHEMISTRY, Issue 1 2002Steve J. Maund
Abstract
The partitioning, bioavailability, and toxicity of cypermethrin in water,sediment systems was investigated.
Cypermethrin adsorbed extensively and rapidly, with an overall mean organic carbon (OC) adsorption partition coefficient (Koc) of 350,000, and approximately 99% adsorption occurred within 24 h. Bioavailability was measured via body burdens of Daphnia magna and Chironomus tentans.
Mean biota,sediment accumulation factors (BSAFs), that is, the concentration in the organism as a proportion of the concentration in the sediment, decreased with increasing OC content.
The BSAF values were 0.31, 0.14, and 0.08 for D. magna and 0.63, 0.19, and 0.08 for C. tentans, in 1, 3, and 13% OC sediments, respectively.
The 10-d median lethal sediment concentrations (LC50s) of cypermethrin were 3.6, 18, and 32 mg/kg for Hyalella azteca and 13, 67, and 62 mg/kg for C. tentans in 1, 3, and 13% OC sediments, respectively.
Predictions of aqueous concentrations at the LC50 in sediments (based on Koc) compared well to each other and to effect concentrations from studies in water alone, suggesting that equilibrium partitioning theory could be used reasonably to predict and normalize the toxicity of cypermethrin across sediments of differing OC content.
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Effects of water hardness and dissolved organic material on bioavailability of selected organic chemicals

ENVIRONMENTAL TOXICOLOGY & CHEMISTRY, Issue 10 2001Jarkko Akkanen
Abstract
The influence of water hardness and dissolved organic matter (DOM) on bioavailability of organic chemicals to Daphnia magna was studied by using benzo[a]pyrene (BaP), pyrene, atrazine, and 3,3,,4,4,-tetrachlorobiphenyl (TCB) as model compounds.
Two types of DOM were used, namely Lake Kontiolampi, Joeusuu, Finland water (KL) and Nordic reference fulvic acid (NoFA) dissolved in artificial freshwater.
Binding of the four contaminants by KL, DOM decreased with increasing water hardness.
Furthermore, increasing hardness reduced the binding of BaP and pyrene to NoFA.
The binding of atrazine and TCB by NoFA was low and was not significantly affected by water hardness.
In the DOM-free samples, the bioconcentration of the four contaminants in D. magna usually was not affected by water hardness.
In the presence of DOM, the bioconcentration factors (BCFs) were lower (except for atrazine) than in the DOM-free controls.
In the presence of both types of DOM, increasing water hardness resulted in higher BCFs for BaP.
The bioconcentration of pyrene and TCB increased with increasing water hardness in the presence of KL DOM.
In conclusion, the effects of DOM and water hardness on bioavailability of hydrophobic chemicals depend on the type of chemical and on the properties of DOM.
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ENVIRONMENTAL TOXICOLOGY & CHEMISTRY, Issue 12 2000George Scott
Abstract
Increasing concentrations of nitrate in surface water and groundwater are becoming a worldwide concern, yet little information has been published on toxicity of nitrate to common organisms used for toxicity testing.
The acute and chronic toxicity of nitrate (NO3 -N) to Ceriodaphnia dubia, Daphnia magna, and Pimephales promelas was investigated in 48-h to 17-d laboratory exposures.
The 48-h median lethal concentration (LC50) of nitrate to C. dubia and D. magna neonates was 374 mg/L NO3 -N and 462 mg/L NO3 -N.
The no-observed-effect concentration (NOEC) and the lowest-observed-effect concentration (LOEC) for neonate production in C. dubia were 21.3 and 42.6 mg/L NO3 -N, respectively.
The NOEC and LOEC values for neonate production in D. magna were 358 and 717 mg/L NO3 -N, respectively.
The 96-h LC50 for larval fathead minnows (P. promelas) was 1, 341 mg/L NO3 -N.
The NOEC and LOEC for 7-d larval and 11-d embryo-larval growth tests were 358 and 717 mg/L NO3 -N, respectively.
Additional exposure of breeding P. promelas and their fertilized eggs to nitrate did not increase susceptibility further.
The LC50 values for all species tested were above ambient concentrations of nitrate reported for surface water.
However, the LOEC for C. dubia was within the range of concentrations that could be found in streams draining areas under extensive agricultural cultivation.
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FRESHWATER BIOLOGY, Issue 1 2009SILVANA SIEHOFF
Summary
1., Daphnia magna, a well-studied primary consumer, is mainly known as a filter feeder.
In this study, we investigated the ability of D. magna to use periphyton as an alternative food source to phytoplankton.
We examined the development of laboratory populations fed with different food sources (Desmodesmus subspicatus and/or periphyton or neither) over a period of 42 days, and observed the behaviour of the daphnids.
2.,The addition of periphyton to phytoplankton food led to an increase of daphnid population biomass.
When fed with periphyton as the only food source, a small but stable D. magna population developed.
3.,The behaviour of daphnids fed with both food sources revealed a preference for feeding on D. subspicatus.
Only below a concentration of D. subspicatus of approximately 0.05 mg C L,1 (0.4 × 107 cells L,1) did D. magna use periphyton as an alternative food source.
4.,Periphyton showed distinct reactions to grazing by D. magna.
The thickness of the periphyton layer was reduced from about 4 to 1 mm and we observed a change in species composition due to grazing.
5.,The ability of D. magna to graze on periphyton could serve to stabilize its population density and reinforce its competitive advantage over other cladocerans.
By switching between food sources, D. magna can act as a coupler between pelagic and benthic habitats and food webs.
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Two hundred years of a diverse Daphnia community in Lake Naivasha (Kenya): effects of natural and human-induced environmental changes

FRESHWATER BIOLOGY, Issue 8 2004Joachim Mergeay
Summary
1. We used fossil diapausing eggs extracted from 210Pb-dated sediment cores to reconstruct historical changes in the Daphnia community of Lake Naivasha, a climate-sensitive lake in Kenya which over the past 200 years has experienced a series of well-documented natural and anthropogenic environmental changes.
2. Contiguous sampling and analysis of four cores yielded ephippial capsules of eight Daphnia species.
Only two of these had been recorded previously in live collections from Lake Naivasha, and one species is new to science.
The four more common species (Daphnia barbata, D. laevis, D. magna, and D. pulex) show striking differences in abundance patterns and population dynamics through time.
Four other species (D. lumholtzi, D. curvirostris, D. longispina s.l., and Daphnia sp. nov. type Limuru.) appear to have been present only occasionally.
Nevertheless, between 1895 and 1915 seven species of Daphnia inhabited Lake Naivasha simultaneously.
3. Despite considerable natural environmental change associated with climate-driven lake-level fluctuations, the Daphnia community of Lake Naivasha has been severely affected by human activities over the past century, especially the introduction of exotic fishes and water-quality changes because of agricultural soil erosion.
The recent reappearance of large-bodied Daphnia species (D. magna, D. barbata, D. lumholtzi, Daphnia sp. nov. type Limuru) after 20,110 years of absence can be explained by their release from fish predation, following a dramatic increase in turbidity caused by excess clastic sediment input from eroded catchment soils.
The small-bodied species D. laevis has fared less well recently, presumably because the benefit of lowered predation pressure is counteracted by more pronounced negative effects of increased turbidity on this species and loss of submerged macrophyte beds which formerly served as predation refuge.
4. Our results suggest that, despite considerable environmental instability and the absence of specialised zooplanktivores, top-down control of fish on large zooplankton is important in Lake Naivasha.
Predation pressure from fish has led to clear-cut shifts in local Daphnia species composition, but failed to drive the larger taxa to extinction.
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Pikeperch Sander lucioperca trapped between niches: foraging performance and prey selection in a piscivore on a planktivore diet

JOURNAL OF FISH BIOLOGY, Issue 4 2008A. Persson
The foraging behaviour of planktivorous pikeperch Sander lucioperca during their first growing season was analysed.
Field data showed that S. lucioperca feed on extremely rare prey at the end of the summer, suggesting the presence of a bottleneck.
In experiments, foraging ability of planktivorous S. lucioperca was determined when fish were feeding on different prey types (Daphnia magna or Chaoborus spp.) and sizes (D. magna of lengths 1 or 2·5 mm) when they occurred alone.
From these results, the minimum density requirement of each prey type was analysed.
The energy gain for three different foraging strategies was estimated; a specialized diet based on either large D. magna or Chaoborus spp. or a generalist diet combining both prey types.
Prey value estimates showed that Chaoborus spp. should be the preferred prey, assuming an energy maximizing principle.
In prey choice experiments, S. lucioperca largely followed this principle, including D. magna in the diet only when the density of the Chaoborus spp. was below a threshold value.
Splitting the foraging bout into different sequences, however, resulted in a somewhat different pattern.
During an initial phase, S. lucioperca captured both prey as encountered and then switched to Chaoborus spp. if prey density was above the threshold level.
The prey selection observed was mainly explained by sampling behaviour and incomplete information about environmental quality, whereas satiation only had marginal effects.
It was concluded that the observed diet based on rare prey items was in accordance with an optimal foraging strategy and may generate positive growth in the absence of prey fish in suitable sizes.
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Influence of UV Radiation on Four Freshwater Invertebrates,

PHOTOCHEMISTRY & PHOTOBIOLOGY, Issue 5 2000Alina Cywinska
ABSTRACT
Laboratory tests confirmed a negative and variable response of the following four species to artificial UV radiation: Cypridopsis vidua, an ostracode; Chironomus riparius, a midge larvae; Hyalella azteca, an amphipod; and Daphnia magna, a daphnid.
Severe damage occurred at UV-B irradiance ranging from 50 to 80% of incident summer values.
Under constant exposure to UV and photosynthetically active radiation (PAR) the acute lethal response was recorded at 0.3, 0.8, 0.8 and 4.9 W m,2 UV-B for D. magna, H. azteca, C. riparius and C. vidua, respectively.
Sublethal UV-B damage to invertebrates included impaired movement, partial paralysis, changes in pigmentation and altered water balance (bloating).
A series of UV-B, UV-A and PAR treatments, applied separately and in combination, revealed a positive role for both UV-A and PAR in slowing down UV-B damage.
Mean lethal concentration values of the species typically more tolerant to UV and PAR (Cypridopsis, Chironomus) decreased conspicuously when both UV-A and PAR were eliminated.
For UV-B,sensitive species (Hyalella, Daphnia) these differences were notably smaller.
We suggest that this gradation of sensitivity among the tested species demonstrates potential differences in repairing mechanisms which seem to work more efficiently for ostracodes and chironomids than for amphipods and daphnids.
Manipulations with a cellulose acetate filter showed that lower range UV-B (280,290 nm), produced by FS-40 lamps, may cause excessive UV damage to invertebrates.
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